1887

Abstract

Despite many ongoing surveillance projects and the recent focus on the veterinary and clinical ‘One Health’ aspects of antimicrobial resistance (AMR), evidence of the extent of any public health risk posed by animal reservoirs with respect to the transmission of resistant strains of to humans remains varied and contentious. In the UK, the main zoonotic reservoir for the foodborne pathogen Shiga toxin-producing (STEC) is cattle and sheep. In this study, we adopt an alternative approach to the risk assessment of transmission of AMR from animals to humans, involving monitoring AMR in isolates of STEC, an established zoonotic, foodborne pathogen, from human cases of gastrointestinal disease.

The aim of this study was to determine the genome-derived AMR profiles for STEC from human cases to assess the risk of transmission of multidrug-resistant STEC from ruminants to humans.

STEC belonging to 10 different clonal complexes (CCs) (=457) isolated from human faecal specimens were sequenced and genome-derived AMR profiles were determined. Phenotypic susceptibility testing was undertaken on all isolates (=100) predicted to be resistant to at least one class of antimicrobial.

Of the 457 isolates, 332 (72.7 %) lacked identifiable resistance genes and were predicted to be fully susceptible to 11 classes of antimicrobials; 125/332 (27.3 %) carried 1 or more resistance genes, of which 83/125 (66.4 %) were resistant to 3 or more classes of antibiotic. The percentage of isolates harbouring AMR determinants varied between CCs, from 4% in CC25 to 100% in CC504. Forty-six different AMR genes were detected, which conferred resistance to eight different antibiotic classes. Resistance to ampicillin, streptomycin, tetracyclines and sulphonamides was most commonly detected. Four isolates were identified as extended-spectrum βlactamase producers. An overall concordance of 97.7 % (=1075/1100) was demonstrated between the phenotypic and genotypic methods.

This analysis provided an indirect assessment of the risk of transmission of AMR gastrointestinal pathogens from animals to humans, and revealed a subset of human isolates of the zoonotic pathogen STEC were resistant to the antimicrobials used in animal husbandry. However, this proportion has not increased over the last three decades, and thismay provide evidence that guidancepromoting responsible practice has been effective.

Funding
This study was supported by the:
  • National Institute for Health Research (Award 109524)
    • Principle Award Recipient: Claire Jenkins
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2020-02-26
2024-04-28
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References

  1. Croxen MA, Law RJ, Scholz R, Keeney KM, Wlodarska M et al. Recent advances in understanding enteric pathogenic Escherichia coli . Clin Microbiol Rev 2013; 26:822–880 [View Article]
    [Google Scholar]
  2. Launders N, Byrne L, Jenkins C, Harker K, Charlett A et al. Disease severity of Shiga toxin-producing E. coli O157 and factors influencing the development of typical haemolytic uraemic syndrome: a retrospective cohort study, 2009–2012. BMJ Open 2016; 6:e009933 [View Article]
    [Google Scholar]
  3. Byrne L, Jenkins C, Launders N, Elson R, Adak GK. The epidemiology, microbiology and clinical impact of Shiga toxin-producing Escherichia coli in England, 2009–2012. Epidemiol Infect 2015; 143:3475–3487 [View Article]
    [Google Scholar]
  4. Sadouki Z, Day MR, Doumith M, Chattaway MA, Dallman TJ et al. Comparison of phenotypic and WGS-derived antimicrobial resistance profiles of Shigella sonnei isolated from cases of diarrhoeal disease in England and Wales, 2015. J Antimicrob Chemother 2017; 72:2496–2502 [View Article]
    [Google Scholar]
  5. Do Nascimento V, Day MR, Doumith M, Hopkins KL, Woodford N et al. Comparison of phenotypic and WGS-derived antimicrobial resistance profiles of enteroaggregative Escherichia coli isolated from cases of diarrhoeal disease in England, 2015–16. J Antimicrob Chemother 2017; 72:3288–3297 [View Article]
    [Google Scholar]
  6. Neuert S, Nair S, Day MR, Doumith M, Ashton PM et al. Prediction of phenotypic antimicrobial resistance profiles from whole genome sequences of non-typhoidal Salmonella enterica . Front Microbiol 2018; 9:592 [View Article]
    [Google Scholar]
  7. Ellington MJ, Ekelund O, Aarestrup FM, Canton R, Doumith M et al. The role of whole genome sequencing in antimicrobial susceptibility testing of bacteria: report from the EUCAST Subcommittee. Clin Microbiol Infect 2017; 23:2–22 [View Article]
    [Google Scholar]
  8. Carroll KJ, Harvey-Vince L, Jenkins C, Mohan K, Balasegaram S. The epidemiology of Shiga toxin-producing Escherichia coli infections in the South East of England: November 2013–March 2017 and significance for clinical and public health. J Med Microbiol 2019; 68:930–939 [View Article]
    [Google Scholar]
  9. Chattaway MA, Dallman TJ, Gentle A, Wright MJ, Long SE et al. Whole genome sequencing for public health surveillance of Shiga toxin-producing Escherichia coli other than serogroup O157. Front Microbiol 2016; 7:258 [View Article]
    [Google Scholar]
  10. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359 [View Article]
    [Google Scholar]
  11. Tewolde R, Dallman T, Schaefer U, Sheppard CL, Ashton P et al. MOST: a modified MLST typing tool based on short read sequencing. PeerJ 2016; 4:e2308 [View Article]
    [Google Scholar]
  12. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25:1754–1760 [View Article]
    [Google Scholar]
  13. Day M, Doumith M, Jenkins C, Dallman TJ, Hopkins KL et al. Antimicrobial resistance in Shiga toxin-producing Escherichia coli serogroups O157 and O26 isolated from human cases of diarrhoeal disease in England, 2015. J Antimicrob Chemother 2017; 72:145–152 [View Article]
    [Google Scholar]
  14. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article]
    [Google Scholar]
  15. McFarland N, Bundle N, Jenkins C, Godbole G, Mikhail A et al. Recurrent seasonal outbreak of an emerging serotype of Shiga toxin-producing Escherichia coli (STEC O55:H7 Stx2a) in the south west of England, July 2014 to September 2015. Euro Surveill 2017; 22: [View Article]
    [Google Scholar]
  16. Willshaw GA, Cheasty T, Smith HR, O'Brien SJ, Adak GK. Verocytotoxin-producing Escherichia coli (VTEC) O157 and other VTEC from human infections in England and Wales: 1995–1998. J Med Microbiol 2001; 50:135–142 [View Article]
    [Google Scholar]
  17. Dallman T, Cross L, Bishop C, Perry N, Olesen B et al. Whole genome sequencing of an unusual serotype of Shiga toxin-producing Escherichia coli . Emerg Infect Dis 2013; 19:1302–1304 [View Article]
    [Google Scholar]
  18. De Rauw K, Thiry D, Caljon B, Saulmont M, Mainil J et al. Characteristics of Shiga toxin producing- and enteropathogenic Escherichia coli of the emerging serotype O80:H2 isolated from humans and diarrhoeic calves in Belgium. Clin Microbiol Infect 2019; 25:111.e5–11111 [View Article]
    [Google Scholar]
  19. Simms I, Gilbart VL, Byrne L, Jenkins C, Adak GK et al. Identification of verocytotoxin-producing Escherichia coli O117:H7 in men who have sex with men, England, November 2013 to August 2014. Euro Surveill 2014; 19:pii: 20946 [View Article]
    [Google Scholar]
  20. Baker KS, Dallman TJ, Ashton PM, Day M, Hughes G et al. Intercontinental dissemination of azithromycin-resistant shigellosis through sexual transmission: a cross-sectional study. Lancet Infect Dis 2015; 15:913–921 [View Article]
    [Google Scholar]
  21. Baker KS, Dallman TJ, Field N, Childs T, Mitchell H et al. Genomic epidemiology of Shigella in the United Kingdom shows transmission of pathogen sublineages and determinants of antimicrobial resistance. Sci Rep 2018; 8:7389 [View Article]
    [Google Scholar]
  22. Mora A, Blanco JE, Blanco M, Alonso MP, Dhabi G et al. Antimicrobial resistance of Shiga toxin (verotoxin)-producing Escherichia coli O157:H7 and non-O157 strains isolated from humans, cattle, sheep and food in Spain. Res Microbiol 2005; 156:793–806 [View Article]
    [Google Scholar]
  23. Cheney TEA, Smith RP, Hutchinson JP, Brunton LA, Pritchard G et al. Cross-sectional survey of antibiotic resistance in Escherichia coli isolated from diseased farm livestock in England and Wales. Epidemiol Infect 2015; 143:2653–2659 [View Article]
    [Google Scholar]
  24. Valat C, Haenni M, Saras E, Auvray F, Forest K et al. CTX-M-15 extended-spectrum β-lactamase in a Shiga toxin-producing Escherichia coli isolate of serotype O111:H8. Appl Environ Microbiol 2012; 78:1308–1309 [View Article]
    [Google Scholar]
  25. Stoesser N, Batty EM, Eyre DW, Morgan M, Wyllie DH et al. Predicting antimicrobial susceptibilities for Escherichia coli and Klebsiella pneumoniae isolates using whole genomic sequence data. J Antimicrob Chemother 2013; 68:2234–2244 [View Article]
    [Google Scholar]
  26. Zankari E, Hasman H, Kaas RS, Seyfarth AM, Agersø Y et al. Genotyping using whole-genome sequencing is a realistic alternative to surveillance based on phenotypic antimicrobial susceptibility testing. J Antimicrob Chemother 2013; 68:771–777 [View Article]
    [Google Scholar]
  27. Ludden C, Raven KE, Jamrozy D, Gouliouris T, Blane B et al. One health genomic surveillance of Escherichia coli demonstrates distinct lineages and mobile genetic elements in isolates from humans versus livestock. MBio 2019; 10:e02693-18 [View Article]
    [Google Scholar]
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